Let's start by reiterating
a little bit of what we know about nutrients, algae and the
functioning of coral reefs. First, living things' rate of
production is often limited by the availability of essential
nutrients, as explored in the first
article in this series. Second, primary production in
the oligotrophic
ocean is low primarily due to the scarcity of certain essential
plant nutrients (usually nitrogen and phosphorus, but iron
and even silicate also play a role) as explored in the second
article in this series. Third, the primary production
over a given area on a coral reef is much higher-an order
of magnitude higher-than the production over a similar area
of ocean even though reef water may have very little more
in the way of dissolved nutrients. So what gives? If the primary
production in the ocean is limited to a low level because
of the scarcity of nutrients in the water, how can the production
on a reef be higher when water with a similar nutrient concentration
is washing over it? In order to support and maintain this
level of production it seems that nutrients would have to
be coming from somewhere and fueling the algae on the reef.
Indeed they are, and one of the important sources of nutrients
such as nitrogen, phosphorus and iron is the terra firma
located very close to most of the world's coral reefs.

Comparing Earth and Ocean

The dry weight
of rich, agricultural soil might be composed of as much as
0.5% nitrogen in the upper layer where plants root themselves
and extract nutrients for growth. In a unit more familiar
to aquarists, that is 5000 ppm. Let us compare this nutrient
concentration to some reported values for seawater over typical
coral reefs (see Table 1).

Nutrient

Reported
range in Ámol/L

Reported
range in ppm

Typical
values in Ámol/L

Typical
values in ppm

Hobbyist-grade
test kit lower-limit of detection in ppm

NH4+

<
2.4

<
0.04

0.05-0.5

0.0009-0.009

0.25

NO3-

0.05-9.8

0.003-0.6

0.05-0.5

0.003-0.03

0.2

PO43-

0.01-0.6

0.001-0.06

0.05-0.3

0.005-0.03

0.03

Table
1. Nutrient concentrations are reported in units
of µmol/L. Because these units may be difficult
for aquarists to interpret, they have also been converted
to ppm and the lower limit of detection with hobbyist
grade test kits has been included as a means of comparison.
Values listed as typical are as interpreted by the author.
These data are pooled from multiple sources (Atkinson,
1987; Crossland and Barnes, 1983; Crossland et al.,
1984; Falter and Sansone, 2000; Furnas et al.,
1995; Johannes et al., 1972; Johannes et al.,
1983; Kinzie III et al., 2001; Lapointe, 1997;
Pilson and Betzer, 1973; Sargent and Austin, 1949; Tribble
et al., 1990; Webb et al., 1975; Szmant
and Forrester, 1996).

As the table shows, the concentration of
nitrogen and phosphorus in oceanic water is much lower than
it is on land, but why? When something dies in the ocean it
begins to sink and decompose, forming the biological pump
as described last month. The nutrients that make up its body
are mineralized and eventually mix or diffuse as widely throughout
the water column as physical forces allow. If something suspended
dies on land it, too, sinks, but through the air. Because
air is not particularly buoyant compared to water, we tend
to call this falling. Without a doubt, any organism of substantial
mass will sink rapidly to the ground and long before it can
fully decompose. It is interesting to wonder how long microscopic
organisms linger in the air after they die, as they often
are as buoyant in the air as many organisms are in the water.
Decomposition of organisms on land, therefore, happens on
and within solid surfaces. As this mineralization of dead
tissue occurs, some nitrogen is lost to the atmosphere as
gaseous ammonia, but much of the nitrogen and phosphorus are
put into the soil or humus where plants can gain access to
them (Bashkin and Howarth, 2003; Schlesinger, 1997). Soil
tends to be shallow compared to the ocean, however. In many
places the soil that receives essentially all of the nutrients
from the mineralization of organic matter may be only a meter
or two deep (or even less sometimes). By comparison, the average
depth of the ocean is 3000 m and varies from zero to more
than 7000 m (Nybakken, 2001). If we compare oceanic water
and terrestrial soil in terms of the sum of their nutrient
content over the range of their depth (perhaps a few meters
for soil and 3000 m on average for the ocean), we find that
they are not so drastically different after all. The major
differences are that the nutrients required for primary production
on land are very concentrated, close to the sunlight, and
can be accessed easily by the primary producers. The nutrients
necessary for primary production in the ocean are much more
diluted due to the larger volume of oceanic water compared
to terrestrial soil, and most of these nutrients are far away
from the photic
zone. This coupling on land of a concentrated source of nutrients
directly adjacent to sunlight allows many terrestrial ecosystems
to support higher levels of productivity over a given area
than the ocean. Land and sea do eventually meet, though. We
must ask, what happens when it rains?

In a Van, Down by the River

, especially if the river is large, we see that during
a heavy storm the water initially remains mostly clear and
the level does not rise. As time passes after the storm the
water rises and possibly becomes more turbid. It eventually
peaks and then begins to fall nearer to the pre-storm level
and degree of turbidity. Exactly when this storm pulse passes
through a floodplain depends on the rate at which the water
goes through headwater streams and tributaries before reaching
that section of river. For example, the Pantanal floodplain
in Brazil floods every year due to rains that begin almost
six months prior to its flooding (Hamilton et al, 1996)!

As we learned in the movie Finding Nemo, "All
drains lead to the ocean." Unfortunately for Nemo, they
usually lead to turbines first This statement is factual,
however, to the extent that any substance that makes its way
into the earth, air or a drainage system on land will eventually
make its way into groundwater or runoff and into the ocean.
Many factors affect how fast and how much of any substance
reaches the ocean, though. Significant amounts of nitrate
and, to a lesser extent, phosphate (orthophosphate has very
low solubility in freshwater), can and do leach from the soil
into headwater streams, into rivers and eventually are flushed
into the ocean. Additionally, depending on land use practices,
variable amounts of sediment may enter a river from its watershed
(Furnas, 2003; Hamilton and Gehrke, 2005). The more rapidly
a river flows, the greater its load and the larger the size
of the particles it can transport. Because many terrigenous
sediments tend to be such concentrated sources of nitrogen
and phosphorus compared to oceanic water, the addition of
these sediments to coastal waters can significantly increase
the availability of nitrogen and phosphorus in such systems.
Therefore, the outwelling of inorganic nitrogen and phosphorus,
primarily as nitrate and orthophosphate, and of organic material
from rivers and land-based runoff, is a critically important
source in the nutrient balance of every coral reef located
near land (Furnas, 2003; Furnas and Mitchell, 1997; Furnas
et al, 1995). The closer a reef is to the terrestrial
environment, the greater the influence that land-based runoff
has on that reef. This influence extends not only hundreds
of meters from shore but, depending on the magnitude of the
input, can influence reef development and nutrient budgets
tens and even hundreds of kilometers away. However, the degree
of influence drops as the distance from land increases. Oceanic
atolls and banks obviously cannot derive nutrient input from
land to the same degree that fringing reefs do, because the
atolls are not located near land. They represent interesting
cases of reef development and will be examined in future installments.
They also comprise only a small portion of the world's total
reef development. Additionally, groundwater enriched with
inorganic nutrients may seep from land through porous frameworks
and onto coral reefs (Lapointe and Matzie, 1996; Shinn et
al, 1994). This pathway's prevalence and importance, however,
is equivocal.

In short, the outwelling of nutrients from land to the coastal
ocean, where most coral reefs are located, is a major factor
in allowing coral reefs to maintain high rates of primary
productivity, as well as large and complex food webs based
on this productivity.

Too Much of a Good Thing

Unfortunately, as
is the case with any natural system, the input of nutrients
to coral reefs from land-based sources, and the balance of
these inputs with rates of sequestration and loss can be,
and have been, perturbed. In the last several decades the
amount of combined nitrogen in the biosphere has doubled
due to human activities (Galloway et al, 1995; Galloway
et al, 2003). Leibig's research on nutrient limitation
and others' research on the processes necessary to fix atmospheric
nitrogen into combined forms led to the development of chemical
fertilizers. This accounts for approximately 57% of anthropogenic
sources of combined nitrogen. The cultivation of N-fixing
crops, such as soybeans and alfalfa to increase soil-N and
thus soil fertility, accounts for about 29% of this increase.
The combustion of fossil fuels accounts for the remaining
14% (Galloway et al, 1995; Galloway et al, 2003).
Phosphorus is mined from mineral deposits and usually is added
along with nitrogen to agricultural fields and urban landscapes
such as lawns and golf courses. It has been estimated that
approximately 25% of anthropogenically fixed nitrogen is exported
to the ocean in riverine water (Howarth et al, 1996;
Conley, 1999). Because of this, most rivers in areas where
fertilization for agriculture and other purposes takes place
have experienced a 2-20-fold increase in the amount of nitrogen
they conduct, and a similar or higher increase in the amount
of phosphorus (Caracao and Cole, 1999; Conley, 1999). This
has been the root of dramatic problems in many areas in the
developed world, and has caused significant eutrophication
of coastal waters in some places.

Perhaps the most dramatic example of nutrient over-enrichment's
effects on a marine ecosystem is the development and expansion
of the "dead zone" in the Gulf of Mexico near the
mouth of the Mississippi River. The Mississippi River watershed
encompasses a significant portion of the United States, especially
its major agricultural region. Fertilization of these agricultural
lands to satisfy world grain markets, which demand high quantities
for low prices, has led to a dramatic increase in the export
of N and P from the watersheds to tributaries of the Mississippi,
eventually to the Mississippi itself and finally to the ocean.
When these nutrients reach the Gulf of Mexico they support
high rates of primary productivity where the rate of production
had previously been lower. The phytoplankton in such areas,
having been alleviated of a normal state of nutrient-limited
production, bloom massively. They, like any organism, die
and contribute to the workings of the biological pump. However,
the decomposition of organic material by bacteria requires
oxygen. Under a scheme of low productivity in the Gulf's surface
waters, the biological oxygen demand (BOD) is low, and the
water remains oxygenated due to low rates of oxygen consumption
by bacteria. As production rises the amount of organic material
decomposing rises and so does the BOD.

Every year as farmers throughout the Mississippi River watershed
fertilize their fields and as suburbanites fertilize their
lawns and support the fertilization of golf courses and other
attractions, the amount of nitrate and phosphate flowing into
the Gulf increases. As it increases, the rate of production
climbs, the BOD follows right behind and an area of hypoxic
water unable to support most marine life (e.g., shrimp, fish,
crabs and bivalves - all of economic and social importance)
grows and grows. This dead zone covers more than 7,000 square
miles-an area the size of New Jersey. This is not the only
hypoxic area in the ocean caused by cultural eutrophication
(indeed, hundreds have been documented), but it is perhaps
the most daunting.

Nutrient-loading on Reefs

Similar eutrophication has occurred
on some coral reefs. The reefs of Kaneohe Bay off Oahu, Hawaii
were severely damaged and nearly destroyed when the outflows
of two major sewage pipes were placed within the bay. Within
a few years the coverage of live stony corals plummeted while
the abundance of macroalgae and certain suspension feeding
and bioeroding organisms increased dramatically. This problem
was worse near the outflows and least noticeable further away.
The cause of the decline in reef health was realized, and
the sewage outflows were moved far offshore into deep water.
Slowly, over the course of years, the reefs began to recover
and are returning to a healthy state.

Uncontrolled release of sewage also severely damaged the
reefs around Jamaica. Again, live coral coverage fell dramatically
and algal cover and abundance increased. While some of Jamaica's
reefs are returning to coral-dominated systems many show no
evidence of recovery to their original state, even after many
years. In fact, it does not appear that some of the reefs
in Jamaica will move in the direction we would consider
recovery any time soon, and instead are remaining in what
may be considered an alternative stable state for this ecosystem.

A major influence on coastal ecosystems that has allowed
the development of many of today's coral reefs is the buffer
provided by mangroves and seagrass beds between land and the
reef. Mangroves and seagrass beds serve as areas of regeneration
for organic material from land, from the reef and from material
produced within each system. They utilize inorganic nutrients
from land in the production of organic material as well. Additionally,
they serve as a source of organic food production for reefs.
Perhaps most importantly they trap fine sediments that stress
reef animals and can lead to reef decline. Unfortunately,
most of these systems have been destroyed throughout the world.
We will examine the importance of mangroves and seagrass beds
in terms of nutrient cycling in a future article in this series.

Alternatively, other reefs such as those off Western Australia
continue substantial growth and development though they experience
significant nutrient enrichment from land-based sources. In
fact, the nutrient concentrations within the water column
on these reefs are often much higher than what has been suggested
as a threshold for algal dominance over corals (Lapointe,
1997; Szmant, 2002). Additionally, the Great Barrier Reef
(hereinafter, GBR) has developed entirely under a case of
increased nutrient input from land due to human activities
(Furnas, 2003). The GBR, before the end of the last ice age,
was merely a thin fringing reef off the Australian continent.
As sea levels rose, the shore moved further west, and the
small fringing reef continued to grow into what it is now.
During this period, however, aboriginal Australians used fire
to clear land in the catchments leading to the GBR lagoon,
and in so doing increased the amount of nutrients and sediment
transported to the GBR lagoon. With the arrival of Europeans
it appears that the transport of sediment to the GBR lagoon
has increased, and as the Northern Territory is developed
for agriculture the export of nutrients to the GBR lagoon
is increasing dramatically (Furnas, 2003). This has caused
some concern about the negative impacts on the GBR of such
increased nutrient abundance and sedimentation. While some
corals seem exceedingly adaptive when it comes to differing
regimes of turbidity and the utilization of autotrophy vs.
heterotrophy, others seem much less tolerant of increasing
turbidity, even if the sediment has the potential to provide
the coral with necessary nutrients (Anthony, 2000; Anthony
and Fabricius, 2000). On the other hand, Anthony (2006) has
just recently published strong evidence suggesting that living
offshore in clear water without the potential stress associated
with sedimentation may prove to be a trade-off for some corals,
compared to living inshore where sedimentation stress is more
likely but where nutrients necessary for growth and reproduction
may be more easily accessed.

Conclusion

Land represents
a major source of the nutrients necessary to fuel coastal
marine ecosystems, including coral reefs. We've seen that
reefs can both benefit from and be destroyed by land-based
runoff. Thus, nutrient enrichment from terrestrial sources
cannot be called either beneficial or deleterious without
context. The outwelling of nutrients can certainly benefit
a reef by allowing it to maintain high levels of primary productivity
and the communities that rely on that productivity, but if
the magnitude of this outwelling is too great or is combined
with other factors (several of which are understood and will
be explored in later segments), these nutrients can also cause
the eutrophication and destruction of that coral reef and,
as in Jamaica, may represent semi-permanent or permanent changes
to the ecosystem. Unfortunately, we have no historical basis
on which to determine which alternate stable state will persist.
Coral reefs use nutrients, though, and they need them in order
to function. The land is one place from which reefs acquire
the nutrients they need, but it certainly is not the only
source that is available or that they utilize. Next month
we will explore other sources of the nutrients that coral
reefs require to continue functioning as they have for millennia.

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